Rectus Femoris: Its Role in Normal Gait

930 Rectus Femoris: ts Role in Normal Gait Thiru M. Annaswamy, MD, Candace J. Giddings, MHA, Ugo Della Croce, PhD, D. Casey Kerrigan, MD ABSTRACT. Annaswamy TM, Giddings CJ, Della Croce U, Kerrigan DC. Rectus femoris: its role in normal gait. Arch Phys Med Rehabil 1999;80:930-4. Objective: To analyze the role of the rectus femoris muscle in nondisabled gait at various walking velocities using fine-wire dynamic electromyography. Design: Descriptive study. Fine-wire electromyography data were collected from the rectus femoris during level walking at four walking speeds. Rectus femoris activity patterns in the loading response phase and the pre- and initial-swing phase of the gait cycle were compared using paired t tests. Setting: A gait laboratory. Subjects: Ten nondisabled adult volunteers. Main Outcome Measures: Amplitude of rectus femoris activity in the loading response phase and the pre- and initial-swing phase during walking at four speeds. Results: There was a bimodal pattern of rectus femoris activity in all subjects, at all speeds, in both phases, with high variability in the onsets, durations, and amplitudes of activity, and paired t tests revealed no significant differences (p >.05) between phases at any walking speed. Conclusion: Activity in the rectus femoris in the pre- and initial-swing phase in nondisabled individuals at all speeds suggests that similar activity detected in individuals with stiff-legged gait may not be inappropriate. 1999 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation S TFF-LEGGED GAT is one of the more common gait disorders in patients with upper motor neuron disorders 17 such as cerebral palsy, 8 incomplete spinal cord injury, 9 stroke, m and traumatic brain injury. The rectus femoris is a two-joint muscle that acts both as a flexor of the hip and as a extensor of the knee. Spasticity in the rectus femoris has been implicated to be one of the causes of stiff-legged gait in patients with upper motor neuron injury. 3-5,8,11-14 The purported theory is that prolonged or inappropriate activity in the rectus femoris during the pre- and initial-swing phase of the gait cycle decreases swing phase knee flexion because of its role as a knee extensor. Reduced knee flexion in swing, on observational analysis, gives From the Harvard Medical School, Department of Physical Medicine and Rehabilitation and Spanlding Rehabilitation Hospital, Boston, MA (Drs. Annaswamy, Della Croce, Kerrigan); the Cattedra Tecnologie Biomediche, Universit~ di Sassari, Sassari, taly (Dr. Della Croce); and The Ohio State University College of Medicine, Columbus, OH (Ms. Giddings). Submitted for publication December 7, 1998. Accepted March 17, 1999. Supported in part by the Public Health Service grant NH HD01071-04 and by the Ellison Foundation. Presented in part at the annual assembly of the American Academy of Physical Medicine and Rehabilitation, November 1997, Atlanta, GA. No commercial party having a direct financial interest in the results of the research supporting this article has or will confer a benefit upon the authors or upon any organization with which the authors are associated. Reprint requests to Thiru M. Annaswamy, MD, Harvard Medical School, Department of Physical Medicine & Rehabilitation, Spaulding Rehabilitation Hospital, Boston, MA 02114. 1999 by the American Congress of Rehabilitation Medicine and the American Academy of Physical Medicine and Rehabilitation 0003-9993/9918008-5353.00/0 such a gait the appearance of a "stiff leg," hence the name. To identify inappropriate, abnormal activity in the rectus femoris, a precise understanding of "normal" rectus femoris activity is necessary. The role of rectus femoris in nondisabled gait has been studied extensively. 5,1518 Most of the studies analyzing the activity patterns of the rectus femoris using dynamic electromyography (EMG) have been done with surface electrodes. 15t9 While the rectus femoris is a relatively superficial muscle, it is surrounded by other heads of the quadriceps femoris (vastii) that are single-joint muscles and act only as extensors of the knee. Cross-talk from the vastii can affect the EMG data picked up by the surface electrodes, thereby resulting in imperfect EMG activity patterns. 2,21 Fine-wire electrodes have been used to record rectus femoris activity because they are highly sensitive in picking up relatively small amounts of activity and highly specific in recording activity from only the muscle in which they are placed. 2,22,23 However, there are few published reports of studies of rectus femoris EMG activity in nondisabled subjects using fine-wire EMG. 2 Patients with stiff-legged gait have a slower walking velocity (<lngsec). 6 t is important to assess whether rectus femoris activity is the cause of slower walking speed or if it primarily serves as a compensation for it. One method of studying this would be to analyze rectus femoris EMG patterns in nondisabled gait at different walking velocities, including very slow speeds. 15-17,24 Another method would be to use computer simulation and modeling of gait. lz25 However, there are no published studies analyzing the role of rectus femoris in nondisabled gait using fine-wire EMG at different speeds of walking. The rectus femoris is active during two phases of the gait cycle. 5,15-18,26 The first burst of activity occurs during the loading response phase of the gait cycle where the rectus femoris acts along with the vastii by acting eccentrically at the knee during load bearing. The second burst of activity occurs during the pre- and initial-swing phase of the gait cycle where the rectus femoris acts as a hip flexor in propelling the limb forward into swing. One study reported that rectus femoris activity during the pre- and initial-swing phase is smaller and insignificant compared with loading response phase activity. 26 A more precise quantitative comparison of the two bursts of activity has not been reported. We conducted a fine-wire EMG study of the rectus femoris to study its role in nondisabled gait with the following objectives: (1) to determine if there is EMG activity in the rectus femoris during the loading response phase as well as the pre- and initial-swing phase of the gait cycle at all walking velocities and (2) to analyze the effects of walking velocity on the pattern of EMG activity in the rectus femoris. METHODS The study was conducted in a gait laboratory. Ten healthy adult volunteers with no history of neurologic or gait disorders were enrolled in the study. The study was approved by our institutional review board and written informed consent was obtained from each subject. Fine-wire electrodes were used to record muscle activity. 27 EMG data were collected on-line) digitized at 2,500Hz, and analyzed off-line (Myosoft soft-

ROLE OF RECTUS FEMORS N NORMAL GAT, Annaswamy 931 Table 1: Paired ttests Between Loading Response Phase and Pre- and nitial-swing Phase -5 () 5 10 15 25 30 %GaitCyde Fig 1. Example of a processed EMG plot from one subject at one walking speed. The linear envelope seen is the ensemble average of the rectus femoris EMG averaged across three channels and three trials, Loading response phase activity was analyzed between -5% and 15% of the gait cycle, and pre- and initial-swing phase activity was analyzed between 50% and 80% of the gait cycle. warea). Foot switches were used to record events during the gait cycle. Three pairs of fine-wire electrodes were placed in each subject's right rectus femoris muscle belly, with one pair each in the proximal, middle, and distal parts of the muscle. Correct placement of the electrodes was tested in the seated position by checking for voluntary muscle activity during (1) resisted isometric hip flexion with a flexed knee and (2) resisted isometric knee extension. Maximum voluntary contraction (MVC) activity was recorded during each of the two maneuvers. EMG activity at rest was recorded at the beginning and end of each study to confirm that there was no resting muscle activity. Foot switches were taped to both feet and programmed to indicate major events during the gait cycle. The subjects walked along a level platform at four preset walking speeds: 0.5m/sec (slow), lm/sec (comfortable), 1.5rrd sec (brisk), and 2m/sec (fast). The order of speeds was selected Walking Speeds* Fast Brisk Comfort Slow Peak activity (%MVC)..17.25.12 Average activity (%MVC).09.13.16.06 * p values are shown. All values are greater than.05. at random. Walking speed was determined by having the subject walk a defined distance while being timed with a stopwatch. A maximum of 10% error in walking velocity was permitted. Each subject was given two to three practice trials for each speed. Three trials were recorded at each speed. There was a 2-minute rest period between speeds. MVC activity was recorded at the end of each subject's study to check for any fatigue effects and to verify that the electrodes were still in place. Data Analysis Raw EMG was processed in a manner similar to the process outlined by Perry and colleaguesy Raw EMG data were sampled at 1,500Hz and postprocessed. They were bandpass filtered (150 to 1,000Hz), rectified, and integrated to provide a linear envelope. 28 All EMG values were then normalized to peak MVC activity. No threshold of EMG activity was stipulated because it was thought that activity at lower speeds might fall under such a stipulated threshold. The normalized EMG values for each subject were then averaged across the three 7 1 60 50-30. m ll [] Fast [] Fast m [] [] rmsnsk i [] Comfort J [] Comfort [ 1NSlow [] Slow P lo. Subject 1 Subject 2 Subject 3 Subject 4 Subject 5 Subject 6 Subject 7 Subject 8 Subject 9 LORP vs. PSP activity Fig 2. Peak activity data from nine subjects at all four walking speeds. For each speed the pair of overlapping columns represents loading response phase (LORP) activity followed by pre- and initial-swing phase (PSP) activity. The relationship between LORP and PSP activity remains the same in each individual across all speeds. (*Data that were not analyzable and therefore omitted). Arch Phys Med Rehabi Vol 80, August 1999

932 ROLE OF RECTUS FEMORS N NORMAL GAT, Annaswamy channels (proximal, middle, and distal) and three trials for each walking speed. Thus, processed EMG data were obtained for each of the four walking speeds per subject. Heel-strike and toe-off events in the gait cycle of the right lower extremity were determined from foot-switch data. Each stride of EMG data was then time normalized and mean EMG values were determined at each percentage point of the gait cycle. The resulting ensemble average of processed EMG data was plotted versus percent gait cycle. This resulted in four plots, representing rectus femoris EMG activity during four walking speeds, for each subject. EMG values were analyzed during two phases. Loading response phase activity was defined as EMG activity occurring between -5% and 15% of the gait cycle. Pre- and initial swing phase activity was defined as EMG activity occurring between 50% and 80% of the gait cycle. The phase intervals used here are slightly longer than standard phase intervals reported in the literature for the preswing and initial swing phases. This was intended to minimize chances of missing normal EMG activity, occurring because of individual variations, outside the standard boundaries for phase intervals. Peak amplitude and average amplitude of EMG activity were computed in the above two phases. Statistical analyses were performed comparing peak and average loading response phase and pre- and initial-swing phase amplitude for each walking speed. RESULTS Analysis of the processed EMG from nine subjects revealed the following information (data from one subject were not analyzable due to poor quality). Bimodal pattern of activity, ie, activity in the loading response and the pre- and initial-swing phaseses, was observed in all 10 subjects at all walking velocities. A sample processed EMG plot is shown in figure 1. Paired t tests between peak loading response phase activity and peak pre- and initial-swing phase activity revealed no significant differences (p >.05) at any walking speed (table 1). Similarly, paired t tests between average loading response phase activity and average pre- and initial-swing phase activity, at each speed of walking, revealed no significant differences (p >.05) (table 1). Using peak activity instead of average activity did not change any study findings. Therefore, those variables were not used distinctly from each other and both were construed to represent amplitude of activity for the purposes of this study. (The terms "activity" or "amplitude of activity" refer to peak EMG activity.) The onset, duration, and amplitude of activity were highly variable across speeds in the same individual. The changes in patterns of activity with walking speed were highly variable across individuals. n other words, there were individual variations in how walking speed affected patterns of activity. However, the relationship between the amplitudes of loading response phase and pre- and initial-swing phase activity was maintained at all speeds in each individual, eg, loading response phase activity was higher than pre- and initial-swing phase activity in subject 5 at all walking speeds. Mean activities of the nine subjects at all four walking speeds are shown in figure 2. Mean activity in the pre- and initial-swing phase was greater than activity in the loading response phase in four subjects and lower than activity in the loading response phase in the other five subjects. Mean and standard deviation of activity in both phases decreased with decreasing walking speeds (fig 3). The mean difference between loading response phase and pre- and initial-swing phase activity and their standard deviations decreased with decreasing walking speeds (fig 4). Comparison of peak MVC activity before and after the study revealed no significant differences ruling out any significant fatigue effects. DSCUSSON We fulfilled our first objective by finding rectus femoris activity in both phases of the gait cycle in nondisabled subjects at all walking velocities. This is in contrast to the findings of Perry and associates 2 who concluded that the rectus femoris is active only during the pre- and initial-swing phase of the gait cycle. n addition, we found that the bursts of activity had highly variable onsets, durations, and amplitudes, which was 60- > 50 30 - T J 10, _ -10,, Fas~LORP Fast/PSP Brisk/LORP Brisk/PSP Comfort/LORP ComforgPSP Activity at various speeds Sow/LORP Slow/PSP Fig 3. Mean ~- 1 SD error bars. Mean and SD decrease with decreasing walking speed. LORP, loading response phase; PSP, pre- and initial-swing phase.

ROLE OF RECTUS FEMORS N NORMAL GAT, Annaswamy 933 30 10 0-10 - - -30 l t Fast Brisk Conlfort Slow Speed of Walking Fig 4. Mean _+ 1 SD error bars of the differences between loading response phase and pre- and initial-swing phase activities are displayed. The means and SDs of the differences between loading response phase and pre- and initial-swing phase activity decrease with decreasing walking speed. similar to findings reported in the literature. 24,29 This indicates that rectus femoris activity during the pre- and initial-swing phase at any walking speed in disabled gait cannot be considered inappropriate. Paired t tests did not reveal any significant difference in activity between phases at any walking speed. This suggests that pre- and initial-swing phase activity can be as substantial as loading response phase activity irrespective of walking speed. Five subjects had higher loading response phase activity than pre- and initial-swing phase activity and four had higher preand initial-swing phase activity than loading response phase activity. The amplitude of activity in both phases decreased with decreasing speeds. This is consistent with previously published studies. 15,16,29,30 The differences and the variation of differences between loading response phase and pre- and initial-swing phase activity decreased with decreasing speeds. Although subjects in our study exhibited activity patterns consistent with previously published studies on normal rectus femoris activity, there was tremendous individual variation, which precluded us from precisely defining normal rectus femoris activity. There might be two distinct patterns of rectus femoris activity: one in which loading response phase activity is more dominant and one in which pre- and initial-swing phase activity may be more dominant. However, to come to such a conclusion, a much larger sample size is required. A more complete description of rectus femoris activity patterns would include analysis of the duration of activity, which was not performed in this study. However, we performed a thorough analysis of the amplitudes of activity, which is critical in determining the role of the rectus femoris in gait; this is the first such study. The subjects walked on a level platform in a gait laboratory, which is an artificial environment. We did not use a metronome to control cadence or a treadmill to control walking speed; these are tools that, if used, could place artificial constraints on the "normality" of walking. rritation from the fine-wire electrodes could potentially induce extraneous muscle activity. Recording EMG at rest, however, revealed no baseline activity, suggesting that the placement of the fine-wire electrodes did not stimulate muscle activity. Determining the functional significance of spasticity in a muscle group requires careful, detailed analysis of all factors that might influence the functional activity. First, what consti- tutes normal activity in a muscle needs to be well established. Second, abnormal activity needs to be assessed in conjunction with the kinematics and kinetics of the activity (in this instance, gait). 12 t is important to distinguish between appropriate, abnormal activity that would serve to compensate for a different primary abnormality from inappropriate, abnormal activity that would be the primary abnormality causing the gait disorder) 1 Piazza and Delp 12 suggested that relatively less rectus femoris activity might be needed in slow walking. No other studies have analyzed rectus femoris activity as a function of walking speed; however, the results of this study suggest that activity patterns in the rectus femoris change with walking speed. Therefore, before characterizing a pattern of activity as inappropriate, it needs to be first ruled out that the activity served as a compensation for slow walking speed. Various surgical techniques aimed at improving gait in patients with stiff-legged gait have focused on eliminating or modifying the action of the rectus femoris on the knee. 3,s,11,21,32 Although there are many reports in the literature of increased knee flexion in swing as a result of these techniques, few have reported any significant improvement in walking velocity. 3,s,32 We propose that one of the factors contributing to the lack of success in improving walking velocity is that these surgical techniques have not addressed the primary abnormality, ie, slow walking speed, and instead have focused their attention on a compensatory activity, ie, abnormal, yet appropriate, rectus femoris activity. Our study results reiterate the importance of assessing muscle activity in conjunction in kinematics and kinetics to determine whether the activity is appropriate or inappropriate. CONCLUSON The rectus femoris is active in both phases of the gait cycle at all walking speeds and the amplitudes in the two phases are not significantly different. Similar patterns of rectus femoris activity in subjects with stiff-legged gait may not be inappropriate. Acknowledgment: The authors thank Thomas Ribaudo, MS, and Mary Todd, BA, for their technical assistance. References 1. Perry J. Contractures. A historical perspective. Clin Orthop Rel Res 1987;219:8-14. 2. Sutherland DH, Larsen LJ, Mann R. Rectus femoris release in selected patients with cerebral palsy: a preliminary report. Dev Med Child Neurol 1975; 17:26-34. 3. Sutherland DH, Santi M, Abel MF. Treatment of stiff-knee gait in cerebral palsy: a comparison by gait analysis of distal rectus femoris transfer versus proximal rectus release. J Pediatr Orthop 1990;10:433-41. 4. Winters TF, Jr, Gage JR, Hicks R. Gait patterns in spastic hemiplegia in children and young adults. J Bone Joint Surg Am 1987;69:437-41. 5. Perry J. Gait analysis: normal and pathological function. Thorofare (NJ): Slack, nc; 1992. 6. Kerrigan DC, Gronley J, Perry J. Stiff-legged gait in spastic paresis: a study of quadriceps and hamstrings muscle activity. Am J Phys Med Rehabil 1991;70:294-300. 7. Kerrigan DC, Sheffler LR. Spastic paretic gait. Crit Rev Phys Med Rehabil 1995;7:253-68. 8. Gage JR, Perry J, Hicks RR, Koop S, Werntz JR. Rectus femoris transfer to improve knee function of children with cerebral palsy. Dev Med Child Neurol 1987;29:159-66. 9. Waters RL, Yakura JS, Adkins R, Barnes G. Determinants of gait performance following spinal cord injury. Arch Phys Med Rehabil 1989;70:811-8. 10. Knutsson E, Richards C. Different types of disturbed motor control in gait of hemiparetic patients. Brain 1979; 102:5-30.

934 ROLE OF RECTUS FEMORS N NORMAL GAT, Annaswamy 11. Perry J. Distal rectus femoris transfer. Dev Med Child Neurol 1987;29:153-8. 12. Piazza SJ, Delp SL. The influence of muscles on knee flexion during the swing phase of gait. J Biomech 1996;29:723-33. 13. Damron TA, Breed AL, Cook T. Diminished knee flexion after hamstring surgery in cerebral palsy patients: prevalence and severity. J Pediatr Orthop B 1993;13:188-91. 14. Sutherland DH, Davids JR. Common gait abnormalities of the knee in cerebral palsy. Clin Orthop Rel Res 1993 ;288:139-47. 15. Murray MP, Mollinger LA, Gardner GM, Sepic SB. Kinematic and EMG patterns during slow, free, and fast walking. J Orthop Res 1984;2:272-80. 16. Shiavi R, Champion S, Freeman F, Griffin P. Variability of electromyographic patterns for level-surface walking through a range of self-selected speeds. Bull Prosth Res 1981;10-35:5-14. 17. Shiavi R, Bugle HJ, Limbird T. Electromyographic gait assessment, Part 1: adult EMG profiles and walking speed. J Rehabil Res Dev 1987;24:13-23. 18. Ericson MO, Nisell R, Ekholm J. Quantified electromyography of lower-limb muscles during level walking. Scand J Rehabil Med 1986;18:159-63. 19. Ounpuu S, DeLuca PA, Bell KJ, Davis RB. Using surface electrodes for the evaluation of the rectus femoris, vastus medialis and vastus lateralis in children with cerebral palsy. Gait Posture 1997;5:211-6.. Perry J, Gronley JK, Bontrager EL. Functional role of the rectus femoris in gait [abstract]. Trans Orthop Res Soc 1989;14:274 21. Chung CY, Stout J, Gage JR. Rectus femoris transfer-gracilis versus Surtorius. Gait Posture 1997;6:137-46. 22. Cicotti MG, Kerlan RK, Perry J, Pink M. An electromyographic analysis of the knee during functional activities; 1. The normal profile. Am J Sports Med 1994;22:645-50. 23. Perry J, Easterday C, Antonelli D. Surface versus intramuscular electrodes for electromyography of superficial and deep muscles. Phys Ther 1981;61:7-15. 24. Shiavi R. Electromyographic patterns in normal adult locomotion. n: Smidt GL, editor. Gait in rehabilitation. New York: Churchill Livingstone; 1990. p. 97-119. 25. Kerrigau DC, Roth RS, Riley PO. The modelling of adult spastic paretic stiff-legged gait swing period based on actual kinematic data. Gait Posture 1998;7:117-24. 26. Csongradi J, Bleck E, Ford WE Gait electromyography in normal and spastic children, with special reference to quadriceps femoris and hamstring muscles. Dev Med Child Neurol 1979;21:738-48. 27. Kerrigan DC, Meister M, Ribaudo TA. A modified technique of preparing disposable fine-wire electrodes. Am J Phys Med Rehabil 1997;76:107-8. 28. Perry J, Bontrager EL, Bogey RA, Gronley JK, Barnes LA. The Rancho EMG analyzer: a computerized system for gait analysis. J Biomed Eng 1993;15:487-96. 29. Shiavi R, Green N, McFadyen B, Frazer M, Chen J. Normative childhood EMG gait patterns. J Orthop Res 1987;5:283-95. 30. Lyons K, Perry J, Gronley JK, Barnes L, Antonelli D. Timing and relative intensity of hip extensor and abductor muscle action during level and stair ambulation. An EMG study. Phys Ther 1983;63:1597-605. 31. Kerrigan DC, Annaswamy TM. The functional significance of spasticity as assessed by gait analysis. J Head Trauma Rehabil 1997;12:29-39. 32. Ounpnu S, Muik E, Davis RB, Gage JR, DeLuca PA. Rectus femoris surgery in children with cerebral palsy. Part : a comparison between the effect of transfer and release of the distal rectus femoris on knee motion. J Pediatr Orthop 1993;13:331-5. Supplier a. Noraxon, nc, 13430 North Scottsdale Road, Suite 104, Scottsdale, AZ. 85254